Vaccine-induced reduction of Helicobacter pylori colonization in mice is interleukin-12 dependent but gamma interferon and inducible nitric oxide synthase independent

Infection and Immunity

Volumn 71, Issue 2, 2003, Pages 910-921

  Garhart, Christine A ^a   Heinzel, Frederick P ^a   Czinn, Steven J ^a   Nedrud, John G ^a  

^a CASE WESTERN RESERVE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CHEMOKINE; CYTOKINE; GAMMA INTERFERON; HELICOBACTER PYLORI VACCINE; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 13; INTERLEUKIN 23; INTERLEUKIN 4; INTERLEUKIN 5; MACROPHAGE INFLAMMATORY PROTEIN 1; MAJOR HISTOCOMPATIBILITY ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; NITRIC OXIDE SYNTHASE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL INFECTION; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE RELEASE; DISEASE ASSOCIATION; FEMALE; GASTRITIS; HELICOBACTER PYLORI; IMMUNIZATION; INFECTION PREVENTION; MAJOR HISTOCOMPATIBILITY COMPLEX; MOUSE; MUCOSAL IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROVOCATION TEST; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; T LYMPHOCYTE; TH2 CELL;

ADMINISTRATION, INTRANASAL; ANIMALS; BACTERIAL VACCINES; FEMALE; GASTRIC MUCOSA; GASTRITIS; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; IMMUNIZATION; INTERFERON TYPE II; INTERLEUKIN-12; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; NITRIC OXIDE SYNTHASE;

EID: 0037306254     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.71.2.910-921.2003     Document Type: Article

References (47)

1. Agnihotri, N., D. Bhasin, H. Vohra, P. Ray, K. Singh, and N. Ganguly. 1998. Characterization of lymphocytic subsets and cytokine production in gastric biopsy samples from Helicobacter pylori patients. Scand. J. Gastroenterol. 33:704-709.
2. Ajuebor, M. N., A. M. Das, L. Virag, R. J. Flower, C. Szabo, and M. Perretti. 1999. Role of resident peritoneal macrophages and mast cells in chemokine production and neutrophil migration in acute inflammation: evidence for an inhibitory loop involving endogenous IL-10. J. Immunol. 162:1685-1691.
3. Bamford, K. B., X. Fan, S. E. Crowe, J. F. Leary, W. K. Gourley, G. K. Luthra, E. G. Brooks, D. Y. Graham, V. E. Reyes, and P. B. Ernst. 1998. Lymphocytes in the human gastric mucosa during Helicobacter pylori have a T helper cell 1 phenotype. Gastroenterology 114:482-492.
4. Blanchard, T. G., S. J. Czinn, R. W. Redline, N. Sigmund, G. Harriman, and J. G. Nedrud. 1999. Antibody-independent protective mucosal immunity to gastric Helicobacter infection in mice. Cell. Immunol. 191:74-80.
5. Cole, S. P., V. F. Kharitonov, and D. G. Guiney. 1999. Effect of nitric oxide on Helicobacter pylori morphology. J. Infect. Dis. 180:1713-1717.
6. Crabtree, J. E., T. M. Shallcross, R. V. Heatley, and J. I. Wyatt. 1991. Mucosal tumour necrosis factor alpha and interleukin-6 in patients with Helicobacter pylori associated gastritis. Gut 32:1473-1477.
7. Crabtree, J. E., J. I. Wyatt, L. K. Trejdosiewicz, P. Peichl, P. H. Nichols, N. Ramsay, J. N. Primrose, and I. J. Lindley. 1994. Interleukin-8 expression in Helicobacter pylori infected, normal, and neoplastic gastroduodenal mucosa. J. Clin. Pathol. 47:61-66.
8. D'Ellos, M. M., M. Manghetti, M. De Carli, F. Costa, C. T. Baldari, D. Burroni, J. L. Telford, S. Romagnani, and G. Del Prete. 1997. T helper 1 effector cells specific for Helicobacter pylori in the gastric antrum of patients with peptic ulcer disease. J. Immunol. 158:962-967.
9. Ermak, T. H., P. J. Giannasca, R. Nichols, G. A. Myers, J. Nedrud, R. Weltzin, C. K. Lee, H. Kleanathous, and T. P. Monath. 1998. Immunization of mice with urease vaccine affords protection against Helicobacter pylori infection in the absence of antibodies and is mediated by MHC class II-restricted responses. J. Exp. Med. 188:2277-2288.
10. Fang, F. C. 1997. Perspectives series: host/pathogen interactions. Mechanisms of nitric oxide-related antimicrobial activity. J. Clin. Invest. 99:2818-2825.
11. Fox, J. G., P. Beck, C. A. Dangler, M. T. Whary, T. C. Wang, H. N. Shi, and C. Nagler-Anderson. 2000. Concurrent enteric helminth infection modulates inflammation and gastric immune responses and reduces helicobacter-induced gastric atrophy. Nat. Med. 6:536-542.
12. Garhart, C. A., R. W. Redline, J. G. Nedrud, and S. J. Czinn. 2002. Clearance of Helicobacter pylori infection and resolution of postimmunization gastritis in a kinetic study of prophylactically immunized mice. Infect. Immun. 70: 3529-3538.
13. Gookin, J. L., J. M. Rhoads, and R. A. Argenzio. 2002. Inducible nitric oxide synthase mediates early epithelial repair of porcine ileum. Am. J. Physiol. Gastrointest. Liver Physiol. 283:G157-G168.
14. Goto, T., A. Nishizono, T. Fujioka, J. Ikewaki, K. Mifune, and M. Nasu. 1999. Local secretory immunoglobulin A and postimmunization gastritis correlate with protection against Helicobacter pylori infection after oral vaccination of mice. Infect. Immun. 67:2531-2539.
15. Gottwein, J. M., T. G. Blanchard, O. S. Targoni, J. C. Eisenberg, B. M. Zagorski, R. W. Redline, J. G. Nedrud, M. Tary-Lehmann, P. V. Lehmann, and S. J. Czinn. 2001. Protective anti-Helicobacter immunity is induced with aluminum hydroxide or complete Freund's adjuvant by systemic immunization. J. Infect. Dis. 184:308-314.
16. Ibraghimov, A., and J. Pappo. 2000. The immune response against Helicobacter pylori - a direct linkage to the development of gastroduodenal disease. Microbes Infect. 2:1073-1077.
17. Ikewaki, J., A. Nishizono, T. Goto, T. Fujioka, and K. Mifune. 2000. Therapeutic oral vaccination induces mucosal immune response sufficient to eliminate long-term Helicobacter pylori infection. Microbiol. Immunol. 44:29-39.
18. Kamradt, A. E., M. Greiner, P. Ghiara, and S. H. Kaufmann. 2000. Helicobacter pylori infection in wild-type and cytokine-deficient C57BL/6 and BALB/c mouse mutants. Microbes Infect. 2:593-597.
19. Karttunen, R. A., T. J. Karttunen, M. M. Yousfi, H. El-Zimaity, D. Y. Graham, and F. El-Zaatari. 1997. Expression of mRNA for interferongamma, interleukin-10, and interleukin-12 (p40) in normal gastric mucosa and in mucosa infected with Helicobacter pylori. Scand. J. Gastroenterol. 32:22-27.
20. Kleanthous, H., G. A. Myers, K. M. Georgakopoulos, T. J. Tibbitts, J. W. Ingrassia, H. L. Gray, R. Ding, Z. Z. Zhang, W. Lei, R. Nichols, C. K. Lee, T. H. Ermak, and T. P. Monath. 1998. Rectal and intranasal immunizations with recombinant urease induce distinct local and serum immune responses in mice and protect against Helicobacter pylori infection. Infect. Immun. 66:2879-2886.
21. Konturek, P. C., T. Brzozowski, Z. Sliwowski, R. Pajdo, J. Stachura, E. G. Hahn, and S. J. Konturek. 1998. Involvement of nitric oxide and prostaglandins in gastroprotection induced by bacterial lipopolysaccharide. Scand. J. Gastroenterol. 33:691-700.
22. Laubach, V. E., E. G. Shesely, O. Smithies, and P. A. Sherman. 1995. Mice lacking inducible nitric oxide synthase are not resistant to lipopolysaccharide-induced death. Proc. Natl. Acad. Sci. USA 92:10688-10692.
23. Lee, A., J. O'Rourke, M. C. De Ungria, B. Robertson, G. Daskalopoulos, and M. F. Dixon. 1997. A standardized mouse model of Helicobacter pylori infection: introducing the Sydney strain. Gastroenterology 112:1386-1397.
24. Lindholm, C., M. Quiding-Jarbrink, H. Lonroth, A. Hamlet, and A. Svennerholm. 1998. Local cytokine response in Helicobacter pylori-infected subjects. Infect. Immun. 66:5964-5971.
25. Lohoff, M., M. Rollinghoff, and F. Sommer. 2000. Helicobacter pylori gastritis: a Th1 mediated disease? J. Biotechnol. 83:33-36.
26. + T cells specific for subunit A of Helicobacter pylori urease reduces H. pylori stomach colonization in mice in the absence of interleukin-4 (IL-4)/IL-13 receptor signaling. Infect. Immun. 69:1714-1721.
27. Metzger, D. W., R. M. McNutt, J. T. Collins, J. M. Buchanan, V. H. Van Cleave, and W. A. Dunnick. 1997. Interleukin-12 acts as an adjuvant for humoral immunity through interferon-gamma-dependent and -independent mechanisms. Eur. J. Immunol. 27:1958-1965.
28. Mohammadi, M., S. Czinn, R. Redline, and J. Nedrud. 1996. Helicobacter-specific cell-mediated immune responses display a predominant TH1 phenotype and promote a DTH response in the stomachs of mice. J. Immunol. 156:4729-4738.
29. Mohammadi, M., J. Nedrud, R. Redline, N. Lycke, and S. Czinn. 1997. Murine CD4 T cell responses to Helicobacter infection: TH1 cells enhance gastritis and TH2 cells reduce bacterial load. Gastroenterology 113:1848-1857.
30. Nathan, C. 1997. Inducible nitric oxide synthase: what difference does it make? J. Clin. Invest. 100:2417-2423.
31. Noach, L. A., N. B. Bosma, J. Jansen, F. J. Hoek, S. J. van Deventer, and G. N. Tytgat. 1994. Mucosal tumor necrosis factor-alpha, interleukin-1 beta, and interleukin-8 production in patients with Helicobacter pylori infection. Scand. J. Gastroenterol. 29:425-429.
32. Oppmann, B., R. Lesley, B. Blom, J. C. Timans, Y. Xu, B. Hunte, F. Vega, N. Yu, J. Wang, K. Singh, F. Zonin, E. Valsberg, T. Churakova, M. Liu, D. Gorman, J. Wagner, S. Zurawski, Y. Liu, J. S. Abrams, K. W. Moore, D. Rennick, R. de Waal-Malefyt, C. Hannum, J. F. Bazan, and R. A. Kastelein. 2000. Novel p19 protein engages IL-12p40 to form a cytokine, IL-23, with biological activities similar as well as distinct from IL-12. Immunity 13:715-725.
33. Pappo, J., D. Torrey, L. Castriotta, A. Savinainen, Z. Kabok, and A. Ibraghimov. 1999. Helicobacter pylori infection in immunized mice lacking major histocompatibility complex class I and class II functions. Infect. Immun. 67:337-341.
34. Pearlman, E., J. Lass, D. Bardenstein, E. Diaconu, F. Hazlett, J. Albright, A. Higgins, and J. Kazura. 1997. IL-12 exacerbates helminth-mediated corneal pathology by augmenting inflammatory cell recruitment and chemokine expression. J. Immunol. 158:827-833.
35. Sawai, N., M. Kita, T. Kodama, T. Tanahashi, Y. Yamaoka, Y.-I. Tagawa, Y. Iwakura, and J. Imanishi. 1999. Role of gamma interferon in Helicobacter pylori-induced gastric inflammatory responses in a mouse model. Infect. Immun. 67:279-285.
36. Shimoyama, T., S. M. Everett, M. F. Dixon, A. T. Axon, and J. E. Crabtree. 1998. Chemokine mRNA expression in gastric mucosa is associated with Helicobacter pylori cagA positivity and severity of gastritis. J. Clin. Pathol. 51:765-770.
37. Simmons, C. P., N. S. Goncalves, M. Ghaem-Maghami, M. Bajaj-Elliott, S. Clare, B. Neves, G. Frankel, G. Dougan, and T. T. MacDonald. 2002. Impaired resistance and enhanced pathology during infection with a noninvasive, attaching-effacing enteric bacterial pathogen, Citrobacter rodentium, in mice lacking IL-12 or IFN-γ. J. Immunol. 168:1804-1812.
38. Smythies, L. E., K. B. Waltes, J. R. Lindsey, P. R. Harris, P. Ghiara, and P. D. Smith. 2000. Helicobacter pylori-induced mucosal inflammation is Th1 mediated and exacerbated in IL-4, but not IFN-gamma, gene-deficient mice. J. Immunol. 165:1022-1029.
39. + lymphocytes in Helicobacter pylori gastritis display a Th1 phenotype. Infect. Immun. 66:5543-5546.
40. Stern, A. S., J. Magram, and D. H. Presky. 1996. Interleukin-12 an integral cytokine in the immune response. Life Sci. 58:639-654.
41. Sutton, P., J. Wilson, and A. Lee. 2000. Further development of the Helicobacter pylori mouse vaccination model. Vaccine 18:2677-2685.
42. Takeuchi, M., M. M. Kosiewicz, P. Alard, and J. W. Streilein. 1997. On the mechanisms by which transforming growth factor-beta 2 alters antigen-presenting abilities of macrophages on T cell activation. Eur. J. Immunol. 27:1648-1656.
43. Trinchieri, G. 1995. Interleukin-12: a proinflammatory cytokine with immunoregulatory functions that bridge innate resistance and antigen-specific adaptive immunity. Annu. Rev. Immunol. 13:251-276.
44. Weltzin, R., H. Kleanthous, F. Guirdkhoo, T. P. Monath, and C. K. Lee. 1997. Novel intranasal immunization techniques for antibody induction and protection of mice against gastric Helicobacter felis infection. Vaccine 15: 370-376.
45. Yamaoka, Y., M. Kita, T. Kodama, N. Sawai, and J. Imanishi. 1996. Helicobacter pylori cagA gene and expression of cytokine messenger RNA in gastric mucosa. Gastroenterology 110:1744-1752.
46. Yamaoka, Y., M. Kita, T. Kodaina, N. Sawai, K. Kashima, and J. Imanishi. 1997. Induction of various cytokines and development of severe mucosal inflammation by cagA gene positive Helicobacter pylori strains. Gut 41:442-451.
47. Yamaoka, Y., M. Kita, T. Kodama, N. Sawai, T. Tanahashi, K. Kashima, and J. Imanishi. 1998. Chemokines in the gastric mucosa in Helicobacter pylori infection. Gut 42:609-617.